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Title: Synergistic Effects of a Chalkophore, Methanobactin, on Microbial Methylation of Mercury

Journal Article · · Applied and Environmental Microbiology
 [1];  [2]; ORCiD logo [3]; ORCiD logo [4];  [5]; ORCiD logo [3];  [6];  [7]; ORCiD logo [5]
  1. Jinan Research Academy of Environmental Sciences, Jinan (China); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Qilu Univ. of Technology, Jinan (China)
  3. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  4. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Old Dominion Univ., Norfolk, VA (United States)
  5. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)
  6. Iowa State Univ., Ames, IA (United States)
  7. Univ. of Michigan, Ann Arbor, MI (United States)

Microbial production of the neurotoxin methylmercury (MeHg) is a significant health and environmental concern, as it can bioaccumulate and biomagnify in the food web. A chalkophore or a copper-binding compound, termed methanobactin (MB), has been shown to form strong complexes with mercury [as Hg(II)] and also enables some methanotrophs to degrade MeHg. It is unknown, however, if Hg(II) binding with MB can also impede Hg(II) methylation by other microbes. Contrary to expectations, MB produced by the methanotrophMethylosinus trichosporiumOB3b (OB3b-MB) enhanced the rate and efficiency of Hg(II) methylation more than that observed with thiol compounds (such as cysteine) by the mercury-methylating bacteriaDesulfovibrio desulfuricansND132 andGeobacter sulfurreducensPCA. Compared to no-MB controls, OB3b-MB decreased the rates of Hg(II) sorption and internalization, but increased methylation by 5- to 7-fold, suggesting that Hg(II) complexation with OB3b-MB facilitated exchange and internal transfer of Hg(II) to the HgcAB proteins required for methylation. Conversely, addition of excess amounts of OB3b-MB or a different form of MB fromMethylocystisstrain SB2 (SB2-MB) inhibited Hg(II) methylation, likely due to greater binding of Hg(II). Collectively, our results underscore the complex roles of microbial exogenous metal-scavenging compounds in controlling net production and bioaccumulation of MeHg in the environment. Some anaerobic microorganisms convert inorganic mercury (Hg) into the neurotoxin methylmercury, which can bioaccumulate and biomagnify in the food web. While the genetic basis of microbial mercury methylation is known, factors that control net methylmercury production in the environment are still poorly understood. Here, it is shown that mercury methylation can be substantially enhanced by one form of an exogenous copper-binding compound (methanobactin) produced by some methanotrophs, but not by another. This novel finding illustrates that complex interactions exist between microbes and that these interactions can potentially affect the net production of methylmercuryin situ.

Research Organization:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States); Univ. of Michigan, Ann Arbor, MI (United States)
Sponsoring Organization:
National Natural Science Foundation of China; National Science Foundation; USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
AC05-00OR22725; SC0018059
OSTI ID:
1615790
Journal Information:
Applied and Environmental Microbiology, Journal Name: Applied and Environmental Microbiology Journal Issue: 11 Vol. 86; ISSN 0099-2240
Publisher:
American Society for MicrobiologyCopyright Statement
Country of Publication:
United States
Language:
English

References (48)

Bioaccumulation of mercury and methylmercury journal February 1995
Isolation of Methanobactin from the Spent Media of Methane-Oxidizing Bacteria book January 2011
Bacterial mercury resistance from atoms to ecosystems journal June 2003
Advanced biotic ligand models: Using surface complexation modeling to quantify metal bioavailability to bacteria in geologic systems journal August 2017
Methane-oxidizing archaea, aerobic methanotrophs and nitrifiers coexist with methane as the sole carbon source journal March 2019
Spectral and thermodynamic properties of Ag(I), Au(III), Cd(II), Co(II), Fe(III), Hg(II), Mn(II), Ni(II), Pb(II), U(IV), and Zn(II) binding by methanobactin from Methylosinus trichosporium OB3b journal December 2006
Mercury binding by methanobactin from Methylocystis strain SB2 journal December 2014
Intracellular Hg(0) Oxidation in Desulfovibrio desulfuricans ND132 journal October 2016
Effects of Cellular Sorption on Mercury Bioavailability and Methylmercury Production by Desulfovibrio desulfuricans ND132 journal November 2016
Contrasting Effects of Dissolved Organic Matter on Mercury Methylation by Geobacter sulfurreducens PCA and Desulfovibrio desulfuricans ND132 journal August 2017
Spectroscopic and Microscopic Evidence of Biomediated HgS Species Formation from Hg(II)–Cysteine Complexes: Implications for Hg(II) Bioavailability journal August 2018
Mercury Sorption and Desorption on Organo-Mineral Particulates as a Source for Microbial Methylation journal January 2019
Mercury Uptake by Desulfovibrio desulfuricans ND132: Passive or Active? journal May 2019
Microbial Biosynthesis of Thiol Compounds: Implications for Speciation, Cellular Uptake, and Methylation of Hg(II) journal June 2019
Stepwise Reduction Approach Reveals Mercury Competitive Binding and Exchange Reactions within Natural Organic Matter and Mixed Organic Ligands journal August 2019
Cysteine Inhibits Mercury Methylation by Geobacter sulfurreducens PCA Mutant Δ omcBESTZ journal April 2015
Thiol-Facilitated Cell Export and Desorption of Methylmercury by Anaerobic Bacteria journal September 2015
Identification of Mercury and Dissolved Organic Matter Complexes Using Ultrahigh Resolution Mass Spectrometry journal December 2016
Nanomolar Copper Enhances Mercury Methylation by Desulfovibrio desulfuricans ND132 journal May 2018
Mercury Adsorption on Minerals and Its Effect on Microbial Methylation journal May 2019
Sulfate stimulation of mercury methylation in freshwater sediments journal November 1992
Human Exposure To Methylmercury through Rice Intake in Mercury Mining Areas, Guizhou Province, China journal January 2008
Mercury Reduction and Cell-Surface Adsorption by Geobacter sulfurreducens PCA journal September 2013
Mercury Methylation by Novel Microorganisms from New Environments journal September 2013
Coupled Mercury–Cell Sorption, Reduction, and Oxidation on Methylmercury Production by Geobacter sulfurreducens PCA journal October 2014
Highly efficient methane biocatalysis revealed in a methanotrophic bacterium journal December 2013
Differentiated availability of geochemical mercury pools controls methylmercury levels in estuarine sediment and biota journal August 2014
Oxidation and methylation of dissolved elemental mercury by anaerobic bacteria journal August 2013
Methanobactin from Methylosinus trichosporium OB3b inhibits N2O reduction in denitrifiers journal January 2018
Predicting the Bioavailability of Metals and Metal Complexes: Critical Review of the Biotic Ligand Model journal January 2005
Whole-ecosystem study shows rapid fish-mercury response to changes in mercury deposition journal September 2007
Mercury reduction and complexation by natural organic matter in anoxic environments journal January 2011
Active transport, substrate specificity, and methylation of Hg(II) in anaerobic bacteria journal May 2011
Methanobactin and MmoD work in concert to act as the ‘copper-switch’ in methanotrophs: Copper-switch in methanotrophy journal May 2013
Methanotrophs and copper journal July 2010
Environmental, genomic and taxonomic perspectives on methanotrophic Verrucomicrobia : Perspectives on methanotrophic journal March 2009
Global prevalence and distribution of genes and microorganisms involved in mercury methylation journal October 2015
Methylmercury uptake and degradation by methanotrophs journal May 2017
The Genetic Basis for Bacterial Mercury Methylation journal February 2013
Detoxification of Mercury by Methanobactin from Methylosinus trichosporium OB3b journal July 2013
Detailed Assessment of the Kinetics of Hg-Cell Association, Hg Methylation, and Methylmercury Degradation in Several Desulfovibrio Species journal August 2012
Metals and Methanotrophy journal January 2018
Sulfate-Reducing Bacterium Desulfovibrio desulfuricans ND132 as a Model for Understanding Bacterial Mercury Methylation journal April 2011
A TonB-Dependent Transporter Is Responsible for Methanobactin Uptake by Methylosinus trichosporium OB3b journal January 2016
Methanobactin and the Link between Copper and Bacterial Methane Oxidation journal March 2016
Mercury bioaccumulation increases with latitude in a coastal marine fish (Atlantic silverside, Menidia menidia ) journal July 2017
High resolution depth distribution of Bacteria, Archaea, methanotrophs, and methanogens in the bulk and rhizosphere soils of a flooded rice paddy journal June 2015
Diversity and Habitat Preferences of Cultivated and Uncultivated Aerobic Methanotrophic Bacteria Evaluated Based on pmoA as Molecular Marker journal December 2015